DOCSLIB.ORG

Differential Depth Distribution of Microbial Function and Putative Symbionts Through Sediment-Hosted Aquifers in the Deep Terrestrial Subsurface

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Differential Depth Distribution of Microbial Function and Putative Symbionts Through Sediment-Hosted Aquifers in the Deep Terrestrial Subsurface ARTICLES https://doi.org/10.1038/s41564-017-0098-y Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface Alexander J. Probst1,5,7, Bethany Ladd2,7, Jessica K. Jarett3, David E. Geller-McGrath1, Christian M. K. Sieber1,3, Joanne B. Emerson1,6, Karthik Anantharaman1, Brian C. Thomas1, Rex R. Malmstrom3, Michaela Stieglmeier4, Andreas Klingl4, Tanja Woyke 3, M. Cathryn Ryan 2* and Jillian F. Banfield 1* An enormous diversity of previously unknown bacteria and archaea has been discovered recently, yet their functional capacities and distributions in the terrestrial subsurface remain uncertain. Here, we continually sampled a CO2-driven geyser (Colorado Plateau, Utah, USA) over its 5-day eruption cycle to test the hypothesis that stratified, sandstone-hosted aquifers sampled over three phases of the eruption cycle have microbial communities that differ both in membership and function. Genome- resolved metagenomics, single-cell genomics and geochemical analyses confirmed this hypothesis and linked microorganisms to groundwater compositions from different depths. Autotrophic Candidatus “Altiarchaeum sp.” and phylogenetically deep- branching nanoarchaea dominate the deepest groundwater. A nanoarchaeon with limited metabolic capacity is inferred to be a potential symbiont of the Ca. “Altiarchaeum”. Candidate Phyla Radiation bacteria are also present in the deepest groundwater and they are relatively abundant in water from intermediate depths. During the recovery phase of the geyser, microaerophilic Fe- and S-oxidizers have high in situ genome replication rates. Autotrophic Sulfurimonas sustained by aerobic sulfide oxidation and with the capacity for N2 fixation dominate the shallow aquifer. Overall, 104 different phylum-level lineages are present in water from these subsurface environments, with uncultivated archaea and bacteria partitioned to the deeper subsurface. uch remains to be learned about how microbial communi­ overlooked due to sampling13 and primer bias13,20,21 and the spatial ties in the deep terrestrial subsurface vary with depth due variation in metabolic functions over depth transects including the Mto limited access to samples without contamination from deep subsurface (100 m below the ground) remains unexplored. drilling fluids or sampling equipment. Studies to date have anal­ Crystal Geyser is a cold­water, CO2­driven geyser located geo­ ysed samples acquired by drilling1–3, from deep mines4,5, subsurface logically within the Paradox Basin, Colorado Plateau, Utah, USA22. research laboratories6,7 and sites of groundwater discharge8–11. These Originally an abandoned oil exploration well, the 800­m deep verti­ investigations have shown that the terrestrial subsurface is popu­ cal borehole has served as a geyser conduit whose regular and sig­ lated by a vast array of previously undescribed archaea and bacteria. nificant flow rate (since 1936) provides uncontaminated access to At one site, an aquifer in Colorado (Rifle, USA), the diversity spans organisms present in underlying aquifers. Prior geological studies much of the tree of life12 and includes organisms of the Candidate have defined the region’s hydrostratigraphy, including the transmis­ Phyla Radiation (CPR)13, which may comprise more than 50% of sive Entrada, Navajo, Wingate and White Rim fractured sandstone all bacterial diversity14, and many other previously undescribed aquifers (listed in order of increasing depth), which are separated by bacterial lineages. Also present in the terrestrial subsurface are low­permeability confining units23,24, through which limited verti­ previously unknown or little known archaea, including members cal connectivity for CO2, water and microbes is largely restricted of the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, to faults and fractures25. A nearby research borehole provided fur­ Nanoarchaeota, Nanohaloarchaea)11,15, Altiarchaeum10, Lokiar­ ther geologic and aquifer geochemical information to 322 m below chaeota16 and Aigarchaeota17. ground surface26. Time­series geochemical data collected over the A major question in subsurface microbiology relates to how ca. 5­day eruption cycle suggest that Crystal Geyser is primarily organisms, and their capacities for carbon, nitrogen and sulfur sourced from the Navajo Sandstone, with increased contributions cycling, vary along depth transects through the terrestrial sub­ from the shallower Entrada Sandstone during major eruptions, and surface. Some evidence pointing to taxonomic variation between increased fraction of deeper water during minor eruptions26,27. 9 m and 52 m below the surface was obtained via a massive A survey of ribosomal proteins predicted from metagenome 16S ribosomal RNA gene survey at the Hanford Site18. Similar sequences from Crystal Geyser microbial communities revealed the variation and change of two functional genes were also detected for existence of a large phylogenetic diversity of previously unknown two shallow aquifers that were accessed via drilling in Germany19. bacteria and archaea in this system8, and a genomic resolution However, major groups of archaea and bacteria may have been study documented a high incidence of carbon­fixation pathways9. 1Department of Earth and Planetary Science, University of California, Berkeley, CA, USA. 2Department of Geoscience, University of Calgary, Calgary, AB, Canada. 3Department of Energy Joint Genome Institute, Walnut Creek, CA, USA. 4Plant Development and Electron Microscopy, Department of Biology I, Biocenter LMU Munich, Planegg-Martinsried, Germany. Present address: 5Present address: Group for Aquatic Microbial Ecology, Biofilm Center, Department of Chemistry, University of Duisburg-Essen, Essen, Germany. 6Present address: Department of Plant Pathology, University of California, Davis, Davis, CA, USA. 7These authors contributed equally: Alexander J. Probst and Bethany Ladd. *e-mail: [email protected]; [email protected] 328 NatURE MICROBIOLOGY | VOL 3 | MARCH 2018 | 328–336 | www.nature.com/naturemicrobiology © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. NATURE MICROBIOLOGY ARTICLES A remaining question relates to the source regions and distribu­ level increased ~3.5 m over 33.5 h, potentially enabling microbes tions of these organisms. Here, we tracked the microbiology and the to thrive in microaerophilic borehole­affected conditions. To sim­ associated geyser discharge geochemistry continuously through­ plify terminology, we henceforth refer to the source water composi­ out the full 5­day geyser eruption cycle to test the hypothesis that tions as relatively ‘deep’ during the minor eruptions, ‘intermediate’ groundwater from stratified aquifers sampled at different stages (and borehole­affected) during the recovery phase and ‘shallow’ of the cycle has microbial communities that differ in both mem­ during the major eruptions. Similar phase variations in the relative bership and function. Our analyses made use of a comprehensive depths of water composition were recently observed27. collection of more than 1,000 newly reconstructed genomes, both Analysis of microbial community composition in the 2015 bulk from metagenomes and single cells, as well as detailed physical and samples made use of a relatively comprehensive database of genomic chemical information that enabled linking of fluids to their ground­ information for the Crystal Geyser system (see Supplementary water source regions. Fig. 2 for sample processing and analysis overview). The genomic dataset included previously reported draft genomes from this system9 Results and new genomes reconstructed from size­fractionated samples Continuous in situ (downhole) monitoring of the geyser water obtained in April and October of 2014 (Supplementary Table 1). pressure throughout the field campaign defined the regular ~5­day Samples included a post­0.2 µ m fraction collected onto a 0.1­µ m period of the eruption cycle (Supplementary Fig. 1). Sampling was filter to enrich for community members with ultra­small cell sizes. conducted over a complete eruption cycle (24–29 May, 2015) dur­ Binning of assembled metagenomes from 27 different samples ing which microbial cells were continuously collected onto 0.1 µ m from five time points in 2014 used seven different algorithms filters. Time series of downhole temperature, electrical conductivity, (see Supplementary Methods) and resulted in 30,574 genomic total dissolved gas pressure and water samples (for major ion, trace bins (with multiple bins for the same genome generated by dif­ metal and dissolved gas analyses) were collected to associate specific ferent algorithms). Selection of the best quality bin generated for microorganisms with water from different geyser eruption intervals any organism in each sample resulted in 5,795 bins for bacteria and relative aquifer depths (Supplementary Fig. 1). and archaea, of which 2,216 were considered to be at least medium Time series of water pressure, electrical conductivity and tem­ quality (> 70% completeness based on single­copy genes with less perature showed three Crystal Geyser eruption phases previously than three multiple single­copy genes). After curation based on observed26,27: the recovery (relatively low water level, no eruptions, guanine­cytosine content, coverage and taxonomy the database light CO2 bubbling), minor eruptions (short eruptions of
Load more

Recommended publications
  • The Syntrophy Hypothesis for the Origin of Eukaryotes Revisited Purificación López-García, David Moreira
    The Syntrophy hypothesis for the origin of eukaryotes revisited Purificación López-García, David Moreira To cite this version: Purificación López-García, David Moreira. The Syntrophy hypothesis for the origin of eukaryotes revisited. Nature Microbiology, Nature Publishing Group, 2020, 5 (5), pp.655-667. 10.1038/s41564- 020-0710-4. hal-02988531 HAL Id: hal-02988531 https://hal.archives-ouvertes.fr/hal-02988531 Submitted on 3 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 2 Perspectives 3 4 5 6 The Syntrophy hypothesis for the origin of eukaryotes revisited 7 8 Purificación López-García1 and David Moreira1 9 10 1 Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France 11 12 13 14 *Correspondence to: [email protected] 15 16 17 18 19 1 20 The discovery of Asgard archaea, phylogenetically closer to eukaryotes than other archaea, together with 21 improved knowledge of microbial ecology impose new constraints on emerging models for the origin of the 22 eukaryotic cell (eukaryogenesis). Long-held views are metamorphosing in favor of symbiogenetic models 23 based on metabolic interactions between archaea and bacteria. These include the classical Searcy’s and 24 hydrogen hypothesis, and the more recent Reverse Flow and Entangle-Engulf-Enslave (E3) models.
    [Show full text]
  • Marsarchaeota Are an Aerobic Archaeal Lineage Abundant in Geothermal Iron Oxide Microbial Mats
    Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats Authors: Zackary J. Jay, Jacob P. Beam, Mansur Dlakic, Douglas B. Rusch, Mark A. Kozubal, and William P. Inskeep This is a postprint of an article that originally appeared in Nature Microbiology on May 14, 2018. The final version can be found at https://dx.doi.org/10.1038/s41564-018-0163-1. Jay, Zackary J. , Jacob P. Beam, Mensur Dlakic, Douglas B. Rusch, Mark A. Kozubal, and William P. Inskeep. "Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats." Nature Microbiology 3, no. 6 (May 2018): 732-740. DOI: 10.1038/ s41564-018-0163-1. Made available through Montana State University’s ScholarWorks scholarworks.montana.edu Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats Zackary J. Jay1,4,7, Jacob P. Beam1,5,7, Mensur Dlakić2, Douglas B. Rusch3, Mark A. Kozubal1,6 and William P. Inskeep 1* The discovery of archaeal lineages is critical to our understanding of the universal tree of life and evolutionary history of the Earth. Geochemically diverse thermal environments in Yellowstone National Park provide unprecedented opportunities for studying archaea in habitats that may represent analogues of early Earth. Here, we report the discovery and character- ization of a phylum-level archaeal lineage proposed and herein referred to as the ‘Marsarchaeota’, after the red planet. The Marsarchaeota contains at least two major subgroups prevalent in acidic, microaerobic geothermal Fe(III) oxide microbial mats across a temperature range from ~50–80 °C. Metagenomics, single-cell sequencing, enrichment culturing and in situ transcrip- tional analyses reveal their biogeochemical role as facultative aerobic chemoorganotrophs that may also mediate the reduction of Fe(III).
    [Show full text]
  • Phylogenomics Provides Robust Support for a Two-Domains Tree of Life
    ARTICLES https://doi.org/10.1038/s41559-019-1040-x Phylogenomics provides robust support for a two-domains tree of life Tom A. Williams! !1*, Cymon J. Cox! !2, Peter G. Foster3, Gergely J. Szöllősi4,5,6 and T. Martin Embley7* Hypotheses about the origin of eukaryotic cells are classically framed within the context of a universal ‘tree of life’ based on conserved core genes. Vigorous ongoing debate about eukaryote origins is based on assertions that the topology of the tree of life depends on the taxa included and the choice and quality of genomic data analysed. Here we have reanalysed the evidence underpinning those claims and apply more data to the question by using supertree and coalescent methods to interrogate >3,000 gene families in archaea and eukaryotes. We find that eukaryotes consistently originate from within the archaea in a two-domains tree when due consideration is given to the fit between model and data. Our analyses support a close relation- ship between eukaryotes and Asgard archaea and identify the Heimdallarchaeota as the current best candidate for the closest archaeal relatives of the eukaryotic nuclear lineage. urrent hypotheses about eukaryotic origins generally pro- Indeed, it has previously been suggested that it is the 3D tree, rather pose at least two partners in that process: a bacterial endo- than the 2D tree, that is an artefact of long-branch attraction5,9–11, symbiont that became the mitochondrion and a host cell for both because analyses under better-fitting models have recovered C 1–4 that endosymbiosis . The identity of the host has been informed a 2D tree but also because the 3D topology is one in which the two by analyses of conserved genes for the transcription and transla- longest branches in the tree of life—the stems leading to bacteria and tion machinery that are considered essential for cellular life5.
    [Show full text]
  • ARCHAEAL EVOLUTION Evolutionary Insights from the Vikings
    RESEARCH HIGHLIGHTS Nature Reviews Microbiology | Published online 16 Jan 2017; doi:10.1038/nrmicro.2016.198 ARCHAEAL EVOLUTION Evolutionary insights from the Vikings The emergence of the eukaryotic cell ASGARD — after the invisible the closest known homologue of during evolution gave rise to all com- ‘Gods of Asgard’ in Norse mythology. eukaryotic epsilon DNA polymerases primordial plex life forms on Earth, including The superphylum consists of the identified thus far. eukaryotic multicellular organisms such as ani- previously identified Lokiarchaeota Members of the ASGARD super- mals, plants and fungi. However, the and Thorarchaeota phyla, and the phylum were particularly enriched vesicular and origin of eukaryotes and their char- newly identified Odinarchaeota and for eukaryotic signature proteins trafficking acteristic structural complexity has Heimdallarchaeota phyla. Using that are involved in intracellular components remained a mystery. The most recent phylogenomics, they discovered trafficking and secretion. Several are derived insights into eukaryogenesis support a strong phylogenetic association proteins contained domain signatures the endosymbiotic theory, which between ASGARD lineages and of eukaryotic transport protein from our proposes that the first eukaryotic eukaryotes that placed the eukaryote particle (TRAPP) complexes, which archaeal cell arose from archaea through the lineage in close proximity to the are involved in transport from the ancestor acquisition of an alphaproteobacterial ASGARD superphylum. endoplasmic
    [Show full text]
  • Two Domains of Life, Not Three?
    Asgard Archaea Two domains of life, not three? A picture of visual interpretation of the Wagner’s opera Das Rheingold, a part of Richard Wagner’s Der Ring des Nibelungen Loki's Castle is a field of five active hydrothermal vents in the mid-Atlantic Ocean, located at 73 degrees north on the Mid-Atlantic Ridge between Greenland and Norway at a depth of 2,352 metres The vents were discovered in 2008 by a multinational scientific expedition of the university of Bergen, and are the most northerly black smokers to date. The five active chimneys of Loki's Castle are venting water as hot as 300 °C and sit on a vast mound of sulfide minerals. The vent field was given the name Loki's Castle as its shape reminded its discoverers of a fantasy castle. The reference is to the ancient Norse god of trickery, Loki. The top three feet (1 m) of a vent chimney almost 40 feet (12 m) tall at Loki's Castle in mid-July 2008. Visible at left is the arm of a remotely operated vehicle, reaching in to take fluid samples. Loki’s Castle Wents Loki's Castle - a field of five active hydrothermal vents in the mid-Atlantic Ocean - at 73 degrees north on the Mid-Atlantic Ridge - at a depth of 2,352 meters In Norse mythology, Loki is a cunning trickster who has the ability to change his shape and sex. Loki is represented as the companion of the great gods Odin and Thor. Preliminary observations have shown the warm area around the Loki's Castle vents to be alive with diverse and apparently unique microorganisms, unlike vent communities observed elsewhere.
    [Show full text]
  • Helarchaeota and Co-Occurring Sulfate-Reducing Bacteria in Subseafloor
    www.nature.com/ismecomms ARTICLE OPEN Helarchaeota and co-occurring sulfate-reducing bacteria in subseafloor sediments from the Costa Rica Margin ✉ Rui Zhao1 and Jennifer F. Biddle 1 © The Author(s) 2021 Deep sediments host many archaeal lineages, including the Asgard superphylum which contains lineages predicted to require syntrophic partnerships. Our knowledge about sedimentary archaeal diversity and their metabolic pathways and syntrophic partners is still very limited. We present here new genomes of Helarchaeota and the co-occurring sulfate-reducing bacteria (SRB) recovered from organic-rich sediments off Costa Rica Margin. Phylogenetic analyses revealed three new metagenome-assembled genomes (MAGs) affiliating with Helarchaeota, each of which has three variants of the methyl-CoM reductase-like (MCR-like) complex that may enable them to oxidize short-chain alkanes anaerobically. These Helarchaeota have no multi-heme cytochromes but have Group 3b and Group 3c [NiFe] hydrogenases, and formate dehydrogenase, and therefore have the capacity to transfer the reducing equivalents (in the forms of hydrogen and formate) generated from alkane oxidation to external partners. We also recovered five MAGs of SRB affiliated with the class of Desulfobacteria, two of which showed relative abundances (represented by genome coverages) positively correlated with those of the three Helarchaeota. Genome analysis suggested that these SRB bacteria have the capacity of H2 and formate utilization and could facilitate electron transfers from other organisms by means of these reduced substances. Their co-occurrence and metabolic features suggest that Helarchaeota may metabolize synergistically with some SRB, and together exert an important influence on the carbon cycle by mitigating the hydrocarbon emission from sediments to the overlying ocean.
    [Show full text]
  • Revealing the Full Biosphere Structure and Versatile Metabolic Functions In
    Chen et al. Genome Biology (2021) 22:207 https://doi.org/10.1186/s13059-021-02408-w RESEARCH Open Access Revealing the full biosphere structure and versatile metabolic functions in the deepest ocean sediment of the Challenger Deep Ping Chen1†, Hui Zhou1,2†, Yanyan Huang3,4†, Zhe Xie5†, Mengjie Zhang1,2†, Yuli Wei5, Jia Li1,2, Yuewei Ma3, Min Luo5, Wenmian Ding3, Junwei Cao5, Tao Jiang1,2, Peng Nan3*, Jiasong Fang5* and Xuan Li1,2* * Correspondence: nanpeng@fudan. edu.cn; [email protected]; lixuan@ Abstract sippe.ac.cn †Ping Chen, Hui Zhou, Yanyan Background: The full biosphere structure and functional exploration of the microbial Huang, Zhe Xie and Mengjie Zhang communities of the Challenger Deep of the Mariana Trench, the deepest known contributed equally to this work. hadal zone on Earth, lag far behind that of other marine realms. 3Ministry of Education Key Laboratory for Biodiversity Science Results: We adopt a deep metagenomics approach to investigate the microbiome and Ecological Engineering, School in the sediment of Challenger Deep, Mariana Trench. We construct 178 of Life Sciences, Fudan University, Shanghai, China metagenome-assembled genomes (MAGs) representing 26 phyla, 16 of which are 5Shanghai Engineering Research reported from hadal sediment for the first time. Based on the MAGs, we find the Center of Hadal Science and microbial community functions are marked by enrichment and prevalence of Technology, College of Marine Sciences, Shanghai Ocean mixotrophy and facultative anaerobic metabolism. The microeukaryotic community is University, Shanghai, China found to be dominated by six fungal groups that are characterized for the first time 1CAS-Key Laboratory of Synthetic in hadal sediment to possess the assimilatory and dissimilatory nitrate/sulfate Biology, CAS Center for Excellence in Molecular Plant Sciences, Institute reduction, and hydrogen sulfide oxidation pathways.
    [Show full text]
  • Metabolic Versatility of the Nitrite-Oxidizing Bacterium Nitrospira
    bioRxiv preprint doi: https://doi.org/10.1101/2020.07.02.185504; this version posted July 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira 2 marina and its proteomic response to oxygen-limited conditions 3 Barbara Bayer1*, Mak A. Saito2, Matthew R. McIlvin2, Sebastian Lücker3, Dawn M. Moran2, 4 Thomas S. Lankiewicz1, Christopher L. Dupont4, and Alyson E. Santoro1* 5 6 1 Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, 7 CA, USA 8 2 Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, 9 Woods Hole, MA, USA 10 3 Department of Microbiology, IWWR, Radboud University, Nijmegen, The Netherlands 11 4 J. Craig Venter Institute, La Jolla, CA, USA 12 13 *Correspondence: 14 Barbara Bayer, Department of Ecology, Evolution and Marine Biology, University of California, 15 Santa Barbara, CA, USA. E-mail: [email protected] 16 Alyson E. Santoro, Department of Ecology, Evolution and Marine Biology, University of 17 California, Santa Barbara, CA, USA. E-mail: [email protected] 18 19 Running title: Genome and proteome of Nitrospira marina 20 21 Competing Interests: The authors declare that they have no conflict of interest. 22 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.02.185504; this version posted July 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
    [Show full text]
  • (Antarctica) Glacial, Basal, and Accretion Ice
    CHARACTERIZATION OF ORGANISMS IN VOSTOK (ANTARCTICA) GLACIAL, BASAL, AND ACCRETION ICE Colby J. Gura A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE December 2019 Committee: Scott O. Rogers, Advisor Helen Michaels Paul Morris © 2019 Colby Gura All Rights Reserved iii ABSTRACT Scott O. Rogers, Advisor Chapter 1: Lake Vostok is named for the nearby Vostok Station located at 78°28’S, 106°48’E and at an elevation of 3,488 m. The lake is covered by a glacier that is approximately 4 km thick and comprised of 4 different types of ice: meteoric, basal, type 1 accretion ice, and type 2 accretion ice. Six samples were derived from the glacial, basal, and accretion ice of the 5G ice core (depths of 2,149 m; 3,501 m; 3,520 m; 3,540 m; 3,569 m; and 3,585 m) and prepared through several processes. The RNA and DNA were extracted from ultracentrifugally concentrated meltwater samples. From the extracted RNA, cDNA was synthesized so the samples could be further manipulated. Both the cDNA and the DNA were amplified through polymerase chain reaction. Ion Torrent primers were attached to the DNA and cDNA and then prepared to be sequenced. Following sequencing the sequences were analyzed using BLAST. Python and Biopython were then used to collect more data and organize the data for manual curation and analysis. Chapter 2: As a result of the glacier and its geographic location, Lake Vostok is an extreme and unique environment that is often compared to Jupiter’s ice-covered moon, Europa.
    [Show full text]
  • Ultradeep Microbial Communities at 4.4 Km Within Crystalline Bedrock: Implications for Habitability in a Planetary Context
    life Article Ultradeep Microbial Communities at 4.4 km within Crystalline Bedrock: Implications for Habitability in a Planetary Context Lotta Purkamo 1,2,* , Riikka Kietäväinen 2,3, Maija Nuppunen-Puputti 4, Malin Bomberg 4 and Claire Cousins 1 1 School of Earth and Environmental Sciences, University of St Andrews, St Andrews KY16 9AL, UK; [email protected] 2 Geological Survey of Finland, 02151 Espoo, Finland; riikka.kietavainen@gtk.fi 3 Department of Geosciences and Geography, University of Helsinki, 00014 Helsinki, Finland 4 VTT Technical Research Centre of Finland, 02044 VTT, Finland; maija.nuppunen-puputti@vtt.fi (M.N.-P.); malin.bomberg@vtt.fi (M.B.) * Correspondence: lotta.purkamo@gtk.fi; Tel.: +358-44-322-9432 Received: 1 November 2019; Accepted: 1 January 2020; Published: 4 January 2020 Abstract: The deep bedrock surroundings are an analog for extraterrestrial habitats for life. In this study, we investigated microbial life within anoxic ultradeep boreholes in Precambrian bedrock, including the adaptation to environmental conditions and lifestyle of these organisms. Samples were collected from Pyhäsalmi mine environment in central Finland and from geothermal drilling wells in Otaniemi, Espoo, in southern Finland. Microbial communities inhabiting the up to 4.4 km deep bedrock were characterized with phylogenetic marker gene (16S rRNA genes and fungal ITS region) amplicon and DNA and cDNA metagenomic sequencing. Functional marker genes (dsrB, mcrA, narG) were quantified with qPCR. Results showed that although crystalline bedrock provides very limited substrates for life, the microbial communities are diverse. Gammaproteobacterial phylotypes were most dominant in both studied sites. Alkanindiges -affiliating OTU was dominating in Pyhäsalmi fluids, while different depths of Otaniemi samples were dominated by Pseudomonas.
    [Show full text]
  • Spatial Separation of Ribosomes and DNA in Asgard Archaeal Cells ✉ ✉ Burak Avcı 1,2 , Jakob Brandt3, Dikla Nachmias4, Natalie Elia4, Mads Albertsen 3, Thijs J
    www.nature.com/ismej BRIEF COMMUNICATION OPEN Spatial separation of ribosomes and DNA in Asgard archaeal cells ✉ ✉ Burak Avcı 1,2 , Jakob Brandt3, Dikla Nachmias4, Natalie Elia4, Mads Albertsen 3, Thijs J. G. Ettema 2, Andreas Schramm1,5 and Kasper Urup Kjeldsen1 © The Author(s) 2021 The origin of the eukaryotic cell is a major open question in biology. Asgard archaea are the closest known prokaryotic relatives of eukaryotes, and their genomes encode various eukaryotic signature proteins, indicating some elements of cellular complexity prior to the emergence of the first eukaryotic cell. Yet, microscopic evidence to demonstrate the cellular structure of uncultivated Asgard archaea in the environment is thus far lacking. We used primer-free sequencing to retrieve 715 almost full-length Loki- and Heimdallarchaeota 16S rRNA sequences and designed novel oligonucleotide probes to visualize their cells in marine sediments (Aarhus Bay, Denmark) using catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH). Super-resolution microscopy revealed 1–2 µm large, coccoid cells, sometimes occurring as aggregates. Remarkably, the DNA staining was spatially separated from ribosome-originated FISH signals by 50–280 nm. This suggests that the genomic material is condensed and spatially distinct in a particular location and could indicate compartmentalization or membrane invagination in Asgard archaeal cells. The ISME Journal; https://doi.org/10.1038/s41396-021-01098-3 INTRODUCTION cells in marine sediments [8] yet methodical limitations did not The origin of the eukaryotic cell is a major unresolved puzzle in allow to discern single cells and to draw any in-depth conclusion the history of life.
    [Show full text]
  • The Bacterial Sulfur Cycle in Expanding Dysoxic and Euxinic Marine Waters
    Environmental Microbiology (2020) 00(00), 00–00 doi:10.1111/1462-2920.15265 Special Issue Article The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters Daan M. van Vliet ,1 F.A. Bastiaan von Meijenfeldt,2 bacteria, and discuss the probable involvement of Bas E. Dutilh,2 Laura Villanueva,3 uncultivated SAR324 and BS-GSO2 bacteria in sulfur Jaap S. Sinninghe Damsté,3,4 Alfons J.M. Stams1,5 oxidation. Uncultivated Marinimicrobia bacteria with and Irene Sánchez-Andrea 1* a presumed organoheterotrophic metabolism are 1Laboratory of Microbiology, Wageningen University and abundant in DMW. Like SRB, they may use specific Research, Stippeneng 4, 6708WE, Wageningen, molybdoenzymes to conserve energy from the oxida- Netherlands. tion, reduction or disproportionation of sulfur cycle 2Theoretical Biology and Bioinformatics, Science for intermediates such as S0 and thiosulfate, produced Life, Utrecht University, Padualaan 8, 3584 CH, Utrecht, from the oxidation of sulfide. We expect that tailored Netherlands. sampling methods and a renewed focus on cultiva- 3Department of Marine Microbiology and tion will yield deeper insight into sulfur-cycling bacte- Biogeochemistry, Royal Netherlands Institute for Sea ria in DMW. Research (NIOZ), Utrecht University, Landsdiep 4, 1797 SZ, ’t Horntje (Texel), Netherlands. Introduction 4Department of Earth Sciences, Faculty of Geosciences, Oxygen deficiency is a rather common phenomenon in Utrecht University, Princetonlaan 8A, 3584 CB, Utrecht, marine waters caused by microbial aerobic respiration Netherlands. coupled to the degradation of organic matter, combined 5Centre of Biological Engineering, University of Minho, with insufficient supply of oxygen through water circulation Campus de Gualtar, 4710-057 Braga, Portugal. or diffusion (Canfield et al., 2005).
    [Show full text]